Dinoflagellate cyst distribution in surface sediments from the South China Sea in relation to hydrographic conditions and primary productivity

Journal Pre-proof Dinoflagellate cyst distribution in surface sediments from the South China Sea in relation to hydrographic conditions and primary productivity

Zhen Li, Vera Pospelova, Hiroshi Kawamura, Chuanxiu Luo, Kenneth Neil Mertens, Ivan Hernández-Almeida, Kedong Yin, Yongsheng Wu, Hui Wu, Rong Xiang PII:

S0377-8398(19)30035-0

DOI:

https://doi.org/10.1016/j.marmicro.2019.101815

Reference:

MARMIC 101815

To appear in:

Marine Micropaleontology

Received date:

12 March 2019

Revised date:

21 November 2019

Accepted date:

7 December 2019

Please cite this article as: Z. Li, V. Pospelova, H. Kawamura, et al., Dinoflagellate cyst distribution in surface sediments from the South China Sea in relation to hydrographic conditions and primary productivity, Marine Micropaleontology(2019), https://doi.org/ 10.1016/j.marmicro.2019.101815

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© 2019 Published by Elsevier.

Journal Pre-proof Dinoflagellate cyst distribution in surface sediments from the South China Sea in relation to hydrographic conditions and primary productivity Zhen Lia* , Vera Pospelovaa,b, Hiroshi Kawamurac, Chuanxiu Luod, Kenneth Neil Mertense, Ivan Hernández-Almeidaf, Kedong Ying, Yongsheng Wuh , Hui Wui, Rong Xiangd

a

School of Earth and Ocean Sciences, University of Victoria, PO Box 1700 STN CSC, Victoria,

Department of Earth and Environmental Sciences, University of Minnesota, 116 Church St SE,

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b

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British Columbia V8W 2Y2, Canada

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Minneapolis, MN 55455, USA

Faculty of Science, Hokkaido University, North 10 West 8, Kita-ku Sapporo 060–0810, Japan

d

CAS Key Laboratory of Marginal Sea Geology, South China Sea Institute of Oceanology,

Ifremer, LER BO, Station de Biologie Marine, Place de la Croix, BP40537, F-29185

Concarneau Cedex, France

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e

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Chinese Academy of Sciences, China

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c

Department of Earth Sciences, ETH Zürich, Sonnegstrasse 5, 8092, Zürich, Switzerland

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School of Marine Sciences, Sun Yat-sen University, Guangzhou, 510275, China

h

Fisheries and Oceans Canada, Bedford Institute of Oceanography, Dartmouth, Nova Scotia

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f

B2Y 4A2, Canada i

State Key Laboratory of Estuarine and Coastal Research, East China Normal University,

Shanghai, China

*Corresponding author: [email protected] Abstract

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Journal Pre-proof The geographical distribution of dinoflagellate cysts was investigated in palynologically treated surface sediments from the South China Sea (SCS) to understand the driving environmental factors associated with specific taxa. The western SCS generally has higher total cyst concentrations (>300 cysts g-1 ) than the eastern region (<200 cysts g-1 ). The highest concentrations (>1000 cysts g-1 ) occur off southern Vietnam, whereas the lowest cyst concentrations are off Luzon. The ratio of heterotrophic to autotrophic taxa has inverse

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distributional patterns to total cyst concentrations, and is likely to be related to an increase in

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relative abundances of autotrophic taxa when nutrient inputs increase.

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Brigantedinium spp., Selenopemphix nephroides, and Stelladinium reidii have their highest

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relative abundances and concentrations off Borneo. Their concentrations are significantly positively correlated with January sea-surface temperature (SST-Jan). In contrast, concentrations undulata,

Spiniferites hyperacanthus,

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of Selenopemphix

Dapsilidinium

pastielsii and

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Operculodinium longispinigerum are negatively correlated with SST-Jan. Lejeunecysta sabrina, cysts of Protoperidinium spp., Votadinium spp., Quinquecuspis concreta and Selenopemphix

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quanta are positively correlated with chlorophyll-a (chl-a) concentrations and are found in the

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high primary productivity regions of the SCS. Total Impagidinium, Impagidinium aculeatum, Impagidinium paradoxum, Impagidinium patulum, Nematosphaeropsis labyrinthus, and Polysphaeridium zoharyi are positively correlated with water depth. Their highest abundances are recorded in the northern slope-deep basin that is influenced by the Kuroshio Current, and this cyst assemblage indicates an open-ocean environment. Key words: Dinoflagellate cysts; South China Sea; Surface sediments; Oceanography; Primary productivity.

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Journal Pre-proof 1. Introduction Dinoflagellates are one of the major groups of modern marine plankton (e.g., Delwiche, 2007). During their life cycle, some dinoflagellates produce resting cysts that can be resistant to physical, chemical and biological degradation, and can fossilize (e.g., Dale, 1996). Distributions of modern marine dinoflagellate cysts are controlled by the sea-surface temperature (SST), seasurface salinity (SSS), nutrient availability, sea- ice cover, and other environmental factors (e.g.,

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Harland, 1983; Dale, 1996; Rochon et al., 1999; de Vernal et al., 2001, 2005; Marret and

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Zonneveld, 2003; Pospelova et al., 2005, 2008; Zonneveld et al., 2013). Therefore, organic-

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walled dinoflagellate cysts are commonly used as indicators of past environmental conditions

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(e.g., Harland, 1973; Lewis et al., 1990; Edwards et al., 1991; Eshet et al., 1994; Rochon et al., 1999; Head et al., 2001; Mudie and Rochon, 2001; Marret and Zonneveld, 2003; 2012;

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Pospelova et al., 2002; Ellegaard et al., 2006; Mohamed et al., 2013; Li et al., 2017; García-

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Moreiras et al., 2018). Some studies use dinoflagellate cyst assemblages especially for qualitative or quantitative reconstructions of SST, SSS, sea-ice cover, or primary productivity

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(PP) (e.g., Mudie et al., 2002; Marret and Zonneveld, 2003; Kawamura, 2004; Pospelova et al.,

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2006, 2015; Ellegaard et al., 2006; Zonneveld et al., 2008; de Vernal et al., 2013; Harland et al., 2013; Price et al., 2013; Bringué et al., 2014; Limoges et al., 2014; Van Nieuwenhove et al. 2016; Li et al., 2017; García-Moreiras et al., 2018). To reconstruct past environmental conditions, it is necessary to know the relationship between individual dinoflagellate cyst species and specific environmental parameters. This requires a good understanding of spatial distributions of cysts in relation to environmental conditions, which can be region-specific (e.g., Dale, 1976, 2009; Pospelova et al., 2004; 2005; Limoges et al., 2010; Shin et al., 2011; Candel et al., 2012; Heikkilä et al., 2014; Price et al., 2016; Gurdebeke et al., 2018).

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Journal Pre-proof Hemispheric and global datasets of dinoflagellate cysts in surface sediments have been assembled to provide detailed information for a better understanding of the environmental drivers of dinoflagellate cyst species at a large basin-scale (e.g., de Vernal et al., 2001; Marret and Zonneveld, 2003; Zonneveld et al., 2013; de Vernal et al., this issue). However, the datasets do not include the South China Sea (SCS), a marginal basin located in the tropical Western Pacific. Influenced by the East Asian Monsoon system, the SCS shows great gradients in

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environmental variables such as SST, SSS, and PP, as well as in eutrophication levels (e.g.,

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Wang and Li, 2009). Therefore, a study of dinoflagellate cysts across the SCS will fill the gap in

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the current dinoflagellate cyst datasets, and will identify the relationships between geographic

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distributions of dinoflagellate cysts in the SCS and specific environmental factors that would also provide adequate information for interpretations of fossil records and paleoenvironmental

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reconstructions.

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Studies of dinoflagellate cysts in surface sediments from the SCS have been carried out along the coast of Guangdong and Fujian Provinces (Qi et al., 1996; Wang et al., 2003; Xiao et

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al., 2003; Wang et al., 2004a, 2004b; Li et al., 2019), the northern shelf-deep basin (Wu and Sun,

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2000), Thailand Gulf and the eastern coast of Malaysia (Lirdwitayaprasit, 1998a; Furio et al., 2006), the Sunda Shelf (Kawamura, 2004), the north-western coast of Borneo (Lirdwitayaprasit, 1998b; Furio et al., 2006), and the west coast of the Philippines (Furio et al., 1996; Azanza et al., 2004; Baula et al., 2011). Most of these studies were focused on morphological descriptions of specific dinoflagellate cyst taxa and their geographical distributions. Li et al. (2019) studied harmful dinoflagellate cysts from 14 surface sediment samples in Daya Bay, an inner fishery bay of Guangdong province. They found that water quality conditions in Daya Bay have a great impact on dinoflagellate cyst distributions. Wu and Sun (2000) studied dinoflagellate cysts from

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Journal Pre-proof 38 surface sediment samples in the northern SCS. However, very low cyst counts and absence of environmental data prevented the authors from exploring a relationship between cysts and factors affecting their distributions. Kawamura (2004) focused on the dinoflagellate cyst distributions on the Sunda Shelf (Figure 1), and provided the first spatial maps of dinoflagellate cysts and discussed potential factors controlling cyst distributions in the area; however, no statistical analyses of water parameters were attempted. In the current study, dinoflagellate cysts in surface

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sediments from the northern and the eastern SCS are investigated. By combining cyst datasets of

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the current study with that of Kawamura (2002, 2004), major distributional patterns of

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dinoflagellate cysts are documented for the entire SCS, with the aim of identifying the

Environmental setting of the SCS

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2.

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environmental parameters driving their regional distribution.

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2.1. Geographic setting

The SCS is one of the largest marginal seas of the western Pacific, surrounded by South

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China, Vietnam, and a chain of islands spanning from Luzon to Borneo (Figure 1). The SCS

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covers an area of ~ 3.5 × 106 km2 and extends from the Tropic of Cancer to the Equator, across > 20 degrees of latitude, consisting of the deep basin (15%), the continental slope (38%), and the continental shelf (47%) (e.g., Wang and Li, 2009). In the deep basin, the water depth averages ∼4,700 m with a maximum of 5,559 m (e.g., Wang and Li, 2009). The slope is positioned between the shelf-break zone and the deep basin, at a water depth of ~300–3700 m. The eastern slope is narrow and steep off Luzon (Figure 1) (e.g., Wang et al., 2008). The continental shelves are well developed in the northern and the southern parts of the SCS, and they tend to become narrower from the west to the east. On the northern shelf, there are numerous submarine deltas

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Journal Pre-proof developed off the Pearl River, the Red River and other smaller rivers. The Sunda Shelf in the southwestern SCS is one of the largest shelves in the world (Figure 1), exceeding ~300 km in width (e.g., Wang and Li, 2009).

2.2. Climatic and oceanographic setting The climate of the SCS region is characterized by the tropical East Asian Monsoon (EAM),

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with the northeast wind dominating in winter (October–April) and the southwest wind in summer

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(May–September) (Figure 2). January is the coldest month when the mean air temperature is

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~15–25 °C, and July is the warmest month with the mean air temperature of ~28 °C. The mean

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annual rainfall for the SCS is ~1000–2000 mm (e.g., Wang and Li, 2009). In general, the SCS displays a pattern of high SST and low SSS in the south while low SST

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and high SSS were observed in the north, likely due to differences in water masses (e.g., Xie et

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al., 2003). SST in the SCS exhibits a strong seasonal cycle, and the maximum SST and minimum SST occur in July and January, respectively (e.g., Xie et al., 2003; Fang et al., 2006) (Figure 3).

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At the study sites, the SST in July ranges from ~27.8 °C to ~30.0 °C, with the highest values

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occurring in the regions off Luzon, Borneo and Hainan, while the lowest SSTs are in the northern coastal areas and upwelling zones (Figure 3 and Table 1). The SSS varies from 28.9 to 34.1 in July and is slightly higher in January from 33.0 to 34.4 (Figure 3 and Table 1), with the highest values documented in January for the northern part, which is influenced by the Kuroshio Current. The lowest values occur in July near river deltas and plumes due to freshwater input (Figure 3). The surface water circulation in the SCS is predominantly wind- forced by the northeast winter and southwest summer monsoons (e.g., Caruso et al., 2006). During winter, this

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Journal Pre-proof circulation is characterized by a basin- wide cyclonic gyre and southwestward coastal currents, whereas in summer, the basin-wide circulation splits into a weakened cyclonic gyre in the north and a strong anti-cyclonic gyre in the south with northeastward coastal currents (Figure 2) (e.g., Qu et al., 2002). The surface waters of the SCS exchange freely with waters from the neighboring seas, while deeper water flows into the SCS primarily from the western Philippine Sea through the Bashi (or Luzon) Strait. The water transport through the Bashi Strait influences

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the circulation and heat budget of the SCS, affecting SST, SSS, circulation, and eddy generation

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in the northeastern SCS (e.g., Wu, 2013). The Kuroshio Current forms to the east of the

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Philippines and flows northward along the coast of Luzon. In general, the Kuroshio tends to

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bypass the Bashi Strait in summer without significant westward intrusion. In winter, the Kuroshio branches into the SCS because of wind stress curl off southwest Taiwan (e.g., Yuan et

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al., 2002; Wu and Hsin, 2012). Typically, the Kuroshio intrusion into the SCS occurs through the

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central region of the Bashi Strait to form anticyclonic circulation in the northeastern SCS. The intrusion occasionally enters the SCS through the northern portion of Bashi Strait and forms a

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cyclonic circulation (e.g., Yuan et al., 2002).

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Upwelling, one of the most important features of sea-surface circulation in the SCS, is induced by winds and is largely affected by local topographic patterns (e.g., Woodson et al., 2007). Upwelling zones have been identified in the regions off southern Vietnam, Hainan and Leizhou Peninsula, South China, southwest of Taiwan, Luzon and northwest of Borneo (Figure 3) (Hu and Wang, 2016). Influenced by monsoons, seasonal variability is a dominant feature of the upwelling in the SCS (Ndah et al., 2016). The Vietnam coastal upwelling zone is located in the shallow region along the eastern and southeastern Vietnam coast, and its cold eddy is off central Vietnam (He et al., 2002; Guo et al., 2006) (Figure 3). The upwelling along the

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Journal Pre-proof northeastern coast of the Hainan Island occurs in summer during the southwest monsoon and is the strongest from mid-July to mid-August (e.g., Jing et al., 2009; Su et al., 2011). The upwelling off Dongshan–Shantou (South China) is driven by the combined effect of wind and topography in summer and is regularly observed in June-September (e.g., Gan et al., 2009). The intrusion of the Kuroshio Current into the northern SCS from the Philippine Sea impinges on the outer shelf of the northern SCS and leads to topographically induced upwelling around the Taiwan Bank and

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the Penghu Islands which may occur at varying strengths year-round (e.g., Hong et al., 2011).

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The upwelling off southwestern Taiwan usually intensifies and peaks between December and

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March (e.g., Ndah et al., 2017). The west Luzon upwelling develops in October-November,

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becomes strong during the intensified northeast monsoon, and decays in February-May (e.g., Yuan et al., 2004). In the southern SCS, winter coastal upwelling has also been identified off

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3. Materials and methods

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and March (e.g., Yan et al., 2015).

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northwest Borneo, and the winter coastal upwelling forms and strengthens between December

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3.1. Sediment collection and environmental parameters A total of 42 surface sediment samples were collected using clamshell grabs (e.g., Van Veen Grab Sampler) from 2008 to 2016 during several research cruises. Samples from the top 1 cm sediments were taken from a container where the grab directly released sediments. These samples cover the northern and the eastern SCS (Figure 1). Dinoflagellate cyst counts and concentration data from 34 surface samples collected in 1997 from the southern and the western SCS (Kawamura 2002, 2004) were included to encompass the entire SCS (Figure 1 and Table 1). Thus, a total of 76 surface samples are from different geographic regions: sample sites 1–11 off

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Journal Pre-proof Luzon, sites 12–16 off Taiwan, sites 17–28 on the northern shelf and in the deep basin off South China, sites 29–35 on the shelf- slope off Hainan, sites 36–53 in the deep basin of the SCS, sites 54–57 on the southern shelf-slope off Borneo, sites 58–64 on the Sunda shelf-slope and sites 65– 76 off southern Vietnam (Figure 1 and Table 1). In general, the sediment types vary from clay to sand (see Table 1 and Figure 4). Sedimentary accumulation rates vary from region to region in the SCS, and the surface

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samples represent different intervals of deposition, depending on the geographic location. The

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accumulation rates recorded in previously studied sediment cores range from 2.5 to 111 cm kyr-1

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in the SCS, with the highest values in the Dongsha area of the northern SCS (Huang et al., 1997;

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Huang and Wang, 1999). The lowest accumulation rates were observed in the slope-deep basin

several hundred years of deposition.

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off Hainan. Therefore, the top surface sediments represent the last several decades or even

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Measured environmental parameters include: water depth (WD), distance to the coastline (DC), monthly averages of chl-a concentrations, SST and SSS in January and July (Chl-a-Jan,

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Chl-a-Jul, SST-Jan, SST-Jul, SSS-Jan and SSS-Jul) and their annual averages from 1997 to 2016

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for all samples (Table 1). Chl-a concentration data were obtained from the global monthly dataset of OCEANCOLOUR_GLO_CHL_L3_REP_OBSERVATIONS_009_065 on a grid of 4 km × 4 km (http://marine.copernicus.eu/services-portfolio/access-to-products). SST and SSS data were acquired from the monthly dataset of GLOBAL_REANALYSIS_PHY_001_030 on a grid of 0.083 × 0.083 degrees (http://marine.copernicus.eu/services-portfolio/access-toproducts/). All the SSSs used here are determined on the practical salinity scale and they have no units according to UNESCO (1985).

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Journal Pre-proof 3.2. Palynological sample preparation and cyst identification Dinoflagellate cysts were extracted using a standard palynological processing technique at the Paleoenvironmental Laboratory at the University of Victoria (e.g., Pospelova et al. 2010). All 42 samples from the northern and the eastern SCS were desalted and oven-dried at ~40 °C, and they were then weighed with an analytical balance. To estimate the concentrations of dinoflagellate cysts, one tablet of Lycopodium clavatum spores (9666 grains per tablet of batch

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no. 3862, University of Lund, Sweden) was added to each sample, except that two tablets were

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added to samples 28 and 29 accidently. The samples were treated with 10% HCl to remove

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carbonates and 48% HF to dissolve silicates at room temperature. Then, a second 10% HCl

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treatment eliminated precipitated fluorosilicates. The samples were rinsed with distilled water and centrifuged after each step. To remove larger and finer particles than cysts, the samples were

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sieved with 120-μm and 15-μm Nitex nylon meshes. A gentle sonication for up to 30s was used

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on samples during sieving (Mertens et al., 2012). Kawamura (2002, 2004) used a similar palynological sample preparation method except for a smaller mesh size (5 μm) and slightly

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lower HF concentrations (40%). The residues were strew- mounted in glycerine jelly between a

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slide and a coverslip. All samples and palynological slides from the current study are stored at the Paleoenvironmental Laboratory, School of Earth and Ocean Sciences, University of Victoria, Canada, and slides from Kawamura (2002, 2004) are housed at the Micropaleontology Group, Institute of Geosciences, Kiel University, Germany. Dinoflagellate cysts were identified and counted using a Nikon Eclipse 80i optical microscope at 400 × or higher magnification. Dinoflagellate cysts were counted in each sample with an average of ~129 cysts. However, the counted number ranges from 0 to 387 cysts due to the large differences in cyst abundances from region to region (Table 1). At least 300 cysts were

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Journal Pre-proof counted when possible, and for those samples with only a few cysts, all cysts were counted in all slides that could be made using the entire sample residue. Our counts of Lycopodium clavatum spores range from 2022 to 11,319 grains per sample. Dinoflagellate cyst identification and motile affinity were determined according to Matsuoka (1988), He and Sun (1991), McMinn (1991), Zhao and Morzadec-Kerfourn (1992a, 1992b, 2004, 2009), Mao and Harland (1993), Kokinos and Anderson (1995), Head (1996),

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Zonneveld et al. (1997), Rochon et al. (1999), Zonneveld and Jurkschat (1999), Esper and

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Zonneveld (2002), Pospelova and Head (2002), Matsuoka et al. (2009), Pospelova and Kim

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(2010), Verleye et al. (2011), Furio et al., (2012), Yu and Morozova (2013), Zonneveld and Pospelova (2015), and Gurdebeke et al. (2019). Cysts were identified to the species level

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whenever possible, but some taxa were grouped into their genus with “spp.” based on their

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morphological similarities. All smooth round brown cysts were grouped as Brigantedinium spp.

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including those with no archeopyle observed and those with a visible archeopyle (e.g., Brigantedinium cariacoense, Brigantedinium irregulare, Brigantedinium simplex). Folded brown

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cysts with obscured horns and/or granulated brown cysts were grouped as cysts of

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Protoperidinium spp. For specimens with similar morphologies to known species but with some minute differences or in cases when some cyst parts were obscure, we added “cf.” to their species names, such as Impagidinium cf. sphaericum, Operculodinium cf. israelianum, Spiniferites cf. ludhamensis, and Cryodinium cf. meridianum. All unspecified Operculodinium species were grouped into Operculodinium spp. Specimens identified as Operculodinium cf. janduchenei (Rochon et al., 1999) and Operculodinium sp. A (Vink, 2000) were grouped into total Operculodinium with all other specimens of Operculodinium for statistical purposes only, but conform to the recently described species Atlanticodinium striaticonulum (Head and

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Journal Pre-proof Mantilla-Duran, this issue). Fifty-eight cyst taxa were identified (Table 2) and most are illustrated in Plates I–III. In this paper, dinoflagellate cysts produced by autotrophic and heterotrophic dinoflagellates are referred to as “autotrophic taxa” and “heterotrophic taxa”, respectively.

3.3. Statistical analysis

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The relative abundances of each dinoflagellate cyst taxon was calculated as its percentage of

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the total counted cysts. The absolute abundances were expressed as concentrations. The

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concentrations of cysts (cysts g-1 ) were calculated using the following formula:

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, where C is the concentration of total or individual dinoflagellate cysts and Ltotal is

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the number of Lycopodium clavatum spores added to the sample. Lcounted and Dcounted are the numbers of counted Lycopodium grains and total cysts or individual dinoflagellate cysts in each

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sample, and G is of the sample in grams dry weight. Golden Software Surfer 10 was used to form

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the contour maps of relative and absolute abundances with the Kriging gridding method of which interpolation was found to give better results for the present dataset than other methods (e.g.,

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Vohat et al., 2013).

To combine the SCS dataset of this study with cyst counts from Kawamura (2002, 2004), the identifications needed to be compared. The most common dinoflagellate cyst taxa were consistent in both datasets: autotrophic taxa were represented by Impagidinium aculeatum, Impagidinium

paradoxum,

Impagidinium

patulum,

Nematosphaeropsis

labyrinthus,

Operculodinium centrocarpum, Operculodinium longispinigerum, Polysphaeridium zoharyi, Spiniferites hyperacanthus, Spiniferites ramosus and Tuberculodinium vancampoae and heterotrophic taxa were represented by Brigantedinium spp., Quinquecuspis concreta, 12

Journal Pre-proof Selenopemphix nephroides, Selenopemphix quanta, Stelladinium reidii and Trinovantedinium applanatum. However, several taxa were identified differently. Based on Kawamura’s illustrations (Plates I–II of Kawamura (2002)), Lingulodinium machaerophorum, Impagidinium strialatum, and Votadinium calvum were here attributed to Lingulodinium sp., Impagidinium sphaericum, and Votadinium spp., respectively (Images 4–5 in Plate I and Image 11 in Plate III in this study). Specimens of Lingulodinium sp. A are considered different from Lingulodinium

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machaerophorum because the former have narrower process bases compared to the middle part

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of the processes, and the tips of the processes are not rounded but sharpened (Image 9 in Plate I)

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(McMinn, 1991). Lingulodinium sp. A also differs from Lingulodinium hemicystum by wider

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middle parts of processes (Images 8–9 in Plate I) (Li et al., 2017). Stelladinium stellatum in Kawamura (2002) was corrected to be Stelladinium reidii in Kawamura (2004). Operculodinium

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israelianum in Kawamura (2002) was identified incorrectly and re- identified as Operculodinium

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sp. -A in Kawamura (2004). This study grouped it into Operculodinium spp. Spiniferites membranaceus wase grouped with Spiniferites mirabilis since we are unable to unambiguously

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identify all specimens in the SCS. To avoid any potential mistakes, some Spiniferites species

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were grouped to the genus level with “.spp” to merge the cyst taxa from the two datasets (Table 3). After grouping, 29 taxa were remained in the combined SCS dataset that was used for cyst distribution and environmental parameter analysis (Table 3). In addition, taxonomical advances allowed more species to be identified or corrected in this study, such as Dubridinium caperatum and Echinidinium aculeatum (Images 6 and 8 in Plate III) which were unidentified in the dataset of Kawamura (2002, 2004). They were directly grouped at the generic level in this study. Cysts of Diplopelta parva are now named as cysts of Niea acanthocysta (Kawami et al., 2006; Liu et al., 2015). The relative abundances of specific cyst taxa in the assemblages from Kawamura

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Journal Pre-proof (2002; 2004) were recalculated after excluding calcareous cysts. Concentrations were also recalculated to cysts per gram of dry weight. Among the 76 samples, most samples have very low cyst concentrations, and only 21 samples have counts with > 200 cysts. For percentage calculations, 38 samples were excluded from statistical analyses since their counts were < 100 cysts (Figure 4). However, they were included in our cyst concentration calculations (Figure 5). Taxa with relative abundances < 1% such as cysts of Alexandrium spp. and cysts of

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Pentapharsodinium dalei were not shown in Figures 4, 5 and 6. Detrended Correspondence

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Analysis (DCA) and Canonical Correspondence Analysis (CCA) were performed to quantify the

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relationship between the environmental parameters and distributional patterns of dinoflagellate

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cysts using CANOCO 4.5 for Windows software (ter Braak and Smilauer, 2002). Since the total counted number of cysts is less than 200 in most of the samples, calculating relative abundances

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may not yield reliable values, especially for rare cyst taxa. Therefore, the concentrations of

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individual dinoflagellate cysts were used to correlate cyst abundances with environmental parameters through DCA and CCA. Dubridinium spp. and Echinidinium spp. were excluded

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from the DCA and CCA since they were not identified in the study of Kawamura (2002, 2004).

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Annual averages of SST, SSS and chl-a concentrations were not included in the environmental variables due to their highly positive correlation with January averages (R=0.98, 0.78, and 0.91, respectively) (Supplementary Table 1). DCA was first applied to test the linear or unimodal character of cyst data variability. The standard deviation of the first DCA gradient was 2.89 for the cyst concentration dataset. The standard deviation was > 2, indicating that dinoflagellate cysts respond to environmental gradients in the unimodal character, justifying the use of CCA (Ter Braak and Prentice, 1988). Forward selection was applied to reduce the set of variables that could effectively explain the

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Journal Pre-proof greatest amount of variance in the dinoflagellate cyst dataset. The relationship between the dinoflagellate cyst distributions and environmental parameters was assessed by species scores and their ordination patterns. Monte Carlo testing was used to determine the significance of each environmental variable. The level of significance of the variables indicates that the environmental variables are strongly related to the species data when P < 0.05.

Results

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4.

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4.1. Dinoflagellate cyst assemblages from different geographic regions

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Twenty-nine cyst taxa were assembled from two datasets, this study and Kawamura (2002,

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2004) (Table 3). The cyst concentrations and assemblages vary from region to region in the SCS (Figures 4 and 5). The region off Luzon has sparse dinoflagellate cysts: no cysts were observed

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at sites 2–5, and only a few were found at sites 6–11 with total cyst concentrations ranging from

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~6 cysts g-1 to ~20 cysts g-1 (Figure 4). Most of the cysts were autotrophic taxa except at site 7. The region off Taiwan is characterized by the highest ratio of heterotrophic to autotrophic

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taxa, ranging from ~4 to 24 and with an average of ~15 (Figure 4). Total cyst concentrations are

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very low in this region and vary from ~29 cysts g-1 to ~139 cysts g-1 . There are only two samples in this area with cyst counts >100 specimens. Brigantedinium spp. comprise ~72% of the assemblages and have an average concentration of ~66 cysts g-1 (Figure 5). A few Impagidinium cysts were found in sediments off Taiwan. The northern shelf- slope off South China has total cyst concentrations ranging from ~14 cysts g-1 to 694 cysts g-1 , with an average of 215 cysts g-1 . The relative abundances of total Spiniferites increase westward from ~20% to ~61%, whereas the abundances of Brigantedinium spp. trend to decrease westward (Figure 4). The autotrophic taxa of Operculodinium

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Journal Pre-proof centrocarpum,

Operculodinium

longispinigerum,

Polysphaeridium

zoharyi,

Spiniferites

hyperacanthus, Spiniferites ramosus and Spiniferites spp. have concentration trends similar to total cyst concentrations (Figure 5). Total Impagidinium cysts have high relative abundances at site 26, whereas the highest concentration of 45 cysts g-1 was observed at site 18 (Figures 4 and 5). In the region off Hainan, concentrations of total dinoflagellate cysts and the relative

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abundances of total Spiniferites increase seaward. In contrast, relative abundances of

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Brigantedinium spp. and cysts of Protoperidinium spp. decrease seaward. Echinidinium spp. also

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decrease from ~13% in nearshore sediments to 0 in offshore sediments, and the highest concentration (43 cysts g-1 ) was observed at coastal site 32 (Figures 4 and 5).

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In the deep basin of the SCS, total cysts concentrations vary from 52 to 630 cysts g-1 . The

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ratios of heterotrophic to autotrophic taxa are very low, with an average of 0.38. Autotrophic

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taxa comprise ~79% of the assemblages, mostly consisting of Operculodinium centrocarpum (~12%), Spiniferites hyperacanthus (~12%), Spiniferites spp. (~10%), total Impagidinium

ur

(~10%), and Spiniferites mirabilis (~5%). The heterotrophic Brigantedinium spp. change from

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0% to 43%, with an average of ~16% (Figure 4). The relative abundances of total Impagidinium have relatively constant values (~15%), and the same applies to Nematosphaeropsis labyrinthus. Concentrations of total Spiniferites,

total Operculodinium,

total Impagidinium

and

Brigantedinium spp. vary from ~10 cysts g-1 to ~211 cysts g-1 , from ~6 cysts g-1 to ~103 cysts g-1, from ~2 cysts g-1 to ~33 cysts g-1 , and from ~0 cysts g-1 to ~190 cysts g-1 , respectively (Figure 5). The southern shelf- slope off Borneo is characterized by sites with relatively high ratios of heterotrophic to autotrophic taxa, averaging 4.18, and has higher concentrations of total cysts (Figure 4). Brigantedinium spp. contribute ~60% to the assemblages, reaching a maximum of

16

Journal Pre-proof ~80% at site 55 where the water depth is ~2000 m. In contrast, the lowest concentrations of the total cysts and Brigantedinium spp. are at site 57 on the shelf with a water depth of 94 m (Figure 5). The Sunda shelf-slope has similar relative abundances of total Spiniferites (~30%) and Brigantedinium spp. (~32%) (Figure 4). Concentrations of Impagidinium cysts are only ~10 cysts g-1 and the relative abundances are from 0% to 2.4% (Figures 4 and 5). The southern

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transect from site 58 to site 61 has lower concentrations and relative abundances of

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Lingulodinium spp. than the northern transect from site 62 to site 64 (Figures 4 and 5).

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The region off southern Vietnam, also the shallowest region, is characterized by the highest total cyst concentrations, ranging from ~30 cysts g-1 to 1371 cysts g-1 and with an average of 494

re

cysts g-1 (Figure 4). In this area, the ratio of heterotrophic to autotrophic taxa ranges from 0.10 to

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0.71, averaging 0.45, and autotrophic taxa comprise 59% to 91% of the assemblages. Spiniferites

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cysts range from ~30% to ~70%, consisting mainly of Spiniferites spp. (~9%), Spiniferites mirabilis (~8%), Spiniferites ramosus

(~8%) and Spiniferites hyperacanthus (~5%).

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Operculodinium centrocarpum and Lingulodinium hemicystum averages are ~9% and ~8%,

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respectively. Brigantedinium spp. dominate heterotrophic taxa and they range from ~7% to ~22%, with an average of ~16% (Figure 4). The concentrations of total Spiniferites, Brigantedinium spp., total Operculodinium, and Lingulodinium hemicystum vary from 12 cysts g1

to 494 cysts g-1 , from 1 cysts g-1 to 197 cysts g-1 , from 38 cysts g-1 to 106 cysts g-1 and from 5

cysts g-1 to 268 cysts g-1 , respectively (Figure 5).

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Journal Pre-proof 4.2. Distribution patterns of dinoflagellate taxa Maps in Figure 6 show spatial distributions of total cyst concentrations, the ratio of heterotrophic to autotrophic taxa, concentrations and relative abundances of heterotrophic, autotrophic and individual cyst taxa. In general, the western SCS has higher total cyst concentrations than the eastern region (Figure 6a). Similar distributional patterns were observed for the concentrations of heterotrophic and autotrophic taxa (Figure 6c and 6d). However, the

of

highest values are highly variable. The region off southern Vietnam has the highest

ro

concentrations of total dinoflagellate cysts and autotrophic taxa (Figure 6a and 6d), whereas the

-p

southern slope off Borneo has the highest concentrations of heterotrophic taxa (Figure 6c). Total

re

cyst concentrations and autotrophic taxa both have the lowest values in the deep er regions off Luzon and Taiwan (Figure 6a and 6d). Relative abundances of heterotrophic taxa range from 0 to

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10% in the northern deep basin and become >80% on the southern slope and in the region off

na

Taiwan (Figure 6c). Autotrophic taxa have the lowest values of both relative abundances and concentrations on the southern slope and in the region off Taiwan and the highest on the slope of

ur

the northern SCS (Figure 6d). The region off Taiwan has the highest ratios of heterotrophic to

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autotrophic taxa (~20), followed by the southern slope off Borneo (~4–6). The ratios are very low in the rest of the SCS (<2) (Figure 6b). Abundances of individual cyst taxa vary greatly. Brigantedinium spp. and total Spiniferites have the highest concentrations of 572 cysts g-1 at site 55 and 494 cysts g-1 at site 71 respectively, followed by total Operculodinium with a maximum of 197 cysts g-1 at site 71 (Figures 5, 6e, 6f and 6g). The highest abundances of Brigantedinium spp. were observed in the region off Borneo, and the relative abundances appear to be high near Taiwan (Figure 6e). Concentration maxima for the rest of dinoflagellate cyst taxa are less than 150 cysts g-1 (Figures 5 and 6).

18

Journal Pre-proof Selenopemphix nephroides and Stelladinium reidii have distributional trends very similar to Brigantedinium spp., except for rather low percentages in the region off Taiwan (Figures 6e, 6n and 6o). The highest concentrations of Votadinium spp., cysts of Protoperidinium spp., Quinquecuspis concreta, and Trinovantedinium applanatum were observed in upwelling influenced coastal waters off southern Vietnam (Figures 6p, 6q and 6r). In general, concentrations and relative abundances of these taxa have similar distributional trends. The

of

highest values of their relative abundances are commonly in the region off Vietnam.

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Echinidinium spp. and Selenopemphix undulata have the highest values of both

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concentrations and percentages in the northern shelf region off South China (Figures 6s and 6t).

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Echinidinium spp. also show high values in the region off Hainan (Figure 6s). In general, Dubridinium spp. were found in low concentrations and relative abundances with the highest

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values of 24 cysts g-1 and ~5% in the deep basin of the southern SCS (Figure 6u).

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Selenopemphix quanta and many autotrophic taxa including Operculodinium centrocarpum, Spiniferites mirabilis, Spiniferites ramosus, Tuberculodinium vancampoae and the relative

ur

abundances of total Lingulodinium have similar distributional patterns: the highest values on the

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northern slope off South China, Hainan, and southern Vietnam, and the lowest in the slope region off Borneo and/or Taiwan (Figures 6h, 6i, 6k, 6l, 6v and 6w). Spiniferites hyperacanthus and Operculodinium longispinigerum have their highest concentrations and relative abundances in the regions off Hainan and South China (Figures 6j and 6x). The former displays the highest values closer to the coastal areas than Operculodinium longispinigerum. High concentrations and

relative abundances of Polysphaeridium zoharyi, total

Impagidinium, Impagidinium aculeatum, Impagidinium paradoxum, Impagidinium patulum, and

19

Journal Pre-proof Nematosphaeropsis labyrinthus were all observed in the deeper parts of the SCS (Figures 6y, 6z, 6aa, 6ab, 6ac, and 6ad). Most of them have the highest values in the slope-deep basin of the northern SCS. Nematosphaeropsis labyrinthus exhibits the highest concentrations (~10 cysts g-1 ) and relative abundances (~3%) in the southern deep basin (Figure 6d). Concentrations of Impagidinium paradoxum have high values in both northern and southern slope-basin regions (Figure 6aa). Dapsilidinium pastielsii was observed in very low abundances (up to 4 cysts g-1 and

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of

~2%) in the slope region off Hainan (Figure 6ae).

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4.3. CCA analysis

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CCA created an ordination in which the first two axes explain 30.7% of the variance in the species data and 85.2% of the variance in the fitted species data (Figure 7). Figure 7 shows that

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SST-Jan (P=0.002), WD (P=0.002), Chl-a-Jul (P=0.002) and SST-Jul (P=0.028) are

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significantly correlated (P<0.05) with the first two CCA axes. Pearson’s linear correlation coefficients of environmental variables show that SST-Jan is slightly positively correlated with

ur

water depth (R=0.52) and negatively with Chl-a-Jul (R=-0.56) (Supplementary Table 1). There is

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no notable correlation among the other parameters (see supplementary material). SSS appears to be less important. The arrow length on the ordination diagram in Figures 7a and 7b indicates the importance of the environmental variables that best explain the dinoflagellate cyst distribution. Therefore, SST-Jan is the most important environmental factor influencing the distribution of dinoflagellate cysts in the SCS. The first axis of the CCA is significantly correlated with SSTJan. Figure 7a shows that the first CCA axis correlates positively with Brigantedinium spp., Selenopemphix nephroides, Stelladinium reidii and Spiniferites bentorii, and negatively with

20

Journal Pre-proof Selenopemphix undulata, Dapsilidinium pastielsii, Operculodinium longispinigerum, and Spiniferites hyperacanthus. The second CCA axis most likely represents SST-Jul, Chl-a-Jul and the WD gradient (Figure 7). The species with the best fit for the negative second axis are cysts of heterotrophic taxa Protoperidinium spp., Lejeunecysta sabrina, Quinquecuspis concreta, Selenopemphix quanta, Trinovantedinium applanatum and Votadinium spp. The species in the positive direction

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of the second CCA axis are Impagidinium spp., Impagidinium patulum, Impagidinium

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paradoxum, Impagidinium aculeatum, Nematosphaeropsis labyrinthus, and Polysphaeridium

-p

zoharyi. Figure 7b shows the sample site scores plotted for the first and the second axes of the

re

CCA and their correlation with the environmental parameters. The scores of the first and the second axes for each site are also plotted on the maps of SST-Jan, SST-Jul, WD, and Chl-a-Jul,

lP

the four significant factors (Figure 8). Sites with the most positive scores on the first axis are in

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the slope-basin of the southern SCS and the region off Taiwan, where SST-Jan is higher (Figure 8a). The most negative values are observed in the slope-basin of the northern SCS where SST-

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Jan is lower (Figure 8a). Sites with the most positive scores of the second axis are in the northern

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slope-basin of the SCS, where SST-Jul is higher and water depth is deeper with lower Chl-a-Jul (Figures 8b, 8c and 8d). In contrast, the sites with the most negative scores are found in the coast-shelf region, where SST-Jul is lower, water is shallower and Chl-a-Jul concentrations are higher. 5. Discussion 5.1. Limitations of data and potential methodological issues It is a common practice for studies of microbial communities to count a minimum number of individuals per sample instead of counting every specimen within a natural system (e.g.,

21

Journal Pre-proof Bennington and Rutherford, 1999). This is based on the fact that statistical analysis using the minimum allowed number of specimens would have similar results as to those obtained using a larger number of specimens. According to statistical comparison studies, 300 individuals per sample are generally required for ecological research (e.g., Chang, 1967; Patterson and Fishbein, 1989; Fatela and Taborda, 2002; Chao et al., 2005). However, when resources are limited, e.g., low absolute abundances of specimens in some samples or a small sample size, it is impossible

of

to count 300 specimens. However, data from a small count can still carry important information.

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For example, after examining 396 datasets, Forcino et al. (2015) found that, depending on the

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evenness of the assemblages, a minimum of 58 specimens per sample can be sufficient to obtain

re

robust results with a broad range of multivariate statistical techniques. In this study, we used absolute cyst abundances (concentrations) rather than relative abundances for all statistical

lP

analysis although it might be acceptable to use cyst counts with >100 specimens for relative

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abundance calculations of the taxa in those samples with low concentrations. Absolute abundance of each dinoflagellate cyst taxon was determined through the counted number of

ur

Lycopodium clavatum spores, thus it has no influence from other taxa. Our counts of

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Lycopodium clavatum grains vary from 2022 to 11,319 per sample, and it is large enough to guarantee that our estimates of cyst concentrations in all samples are reliable for the analysis. To study relationships between dinoflagellate cysts in surface sediments (~ 0–1 cm) and environmental parameters, it is desirable to have water quality parameters measured for the entire duration of cyst accumulations in all samples. However, sediment accumulation rates on the seafloor are different from site to site. In the SCS, the accumulation rates vary from a decade in the near-shore sites to a few hundreds of years in the deep-offshore sites. The available water quality data only go back as far as 1997, and encompass the depositional intervals for some but

22

Journal Pre-proof not all samples. This could potentially lead to some discrepancies in the estimated values for measured environmental parameters and their impact on cyst distributions.

5.2. Concentrations of total dinoflagellate cysts and heterotrophic taxa related to upwe lling of the SCS Upwelling usually intensifies the vertical water exchange and brings nutrient-rich deep

of

waters to the surface, which results in high levels of PP and dinoflagellate production (e.g.,

ro

Smayda and Trainer, 2010). Many regions of active upwelling are characterized by high

-p

dinoflagellate cyst concentrations (e.g., Eshet et al., 1994; Marret, 1994; Dale, 1996, 2002;

re

Marret and Zonneveld, 2003; Sprangers et al., 2004; Holzwarth et al., 2007; Pospelova et al., 2008; Bringué et al., 2013). In the water column, the most intense dinoflagellate production was

lP

reported on the edge of upwelling cells rather than within the cell itself (e.g., Smayda and

na

Trainer, 2010). However, our study shows that cyst concentrations are higher in the shelf-break zone than at the sites near coastal upwelling zones off South China and Hainan (Figure 6a). A

ur

similar distributional pattern was also observed in the middle Atlantic Bight Shelf (e.g., Lee et

Jo

al., 1991) and the East China Sea (e.g., Wong et al., 2004) where high PP is induced by nutrients from deep waters due to intensified upwelling along the shelf-break where the shelf is wide (e.g., Benthuysen et al., 2014). Upwelling along the shelf-break zone is usually triggered by a rapid change in the bathymetry gradient creating a higher pressure gradient (e.g., Hill and Johnson, 1974; Lill, 1979; Matano and Palma, 2008; Benthuysen et al., 2014). This interpretation seems unreasonable for the SCS because of a lack of shelf-break upwelling in the northern SCS. In contrast, the SCS has a shallow mixed- layer with a depth of ~40 m in summer and of ~70 m in winter, much shallower than the shelf-break water depth of 100–120 m (e.g., Wong et al., 2015).

23

Journal Pre-proof Southward to the adjacent open sea, the mixed layer depth becomes shallower at ~20 m in summer (e.g., Wong et al., 2007). Wong et al. (2015) interpreted that colder upper nutrient thermocline or nutricline waters below the shallower mixed-layer of the open SCS can extend freely on to the shelf of the northern SCS. This may increase nutrient concentrations landward from the shelf-break zone to the shelf. Internal waves could enhance the vertical mixing and transfer the cold and nutrient-rich waters to the surface mixed layer and fuel primary productivity

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(e.g., Pan et al., 2012).

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On the other hand, the distribution of dinoflagellate cysts in the sediments is not only

-p

determined by the ecology of dinoflagellates, but also can be influenced by transport processes

re

and preservation conditions (e.g., Dale, 1996; Zonneveld and Brummer, 2000; Zonneveld et al., 2013). Cysts may be transported by ocean currents as they sink through the water column or be

lP

resuspended by bottom currents and mass flows after deposition (e.g., Dale, 1976; Zonneveld

na

and Brummer, 2000). Dinoflagellate cysts are generally thought to behave like silt particles in the water column because their size is within the silt range (e.g., Dale, 1976, 1996; Anderson and

ur

Lively, 1985; Mudie and Harland, 1996). Cysts on the shelf of the SCS could be transported by

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internal solitary waves that can induce and suspend large amounts of sediments from shelf to deep-sea areas of the northern South China Sea (Jia et al., 2019) and be deposited in the deeper part of the basin. Kawamura (2004) suggested that the low cyst concentrations in the Sunda Shelf sediments are mainly controlled by sediment transport and winnowing processes. In this study, the lowest cyst concentrations are observed at sites 20–22 28, 57–58, 61–62 and 67 where sediments are coarser than silt and cysts are perhaps transported away by local currents (Figure 4).

24

Journal Pre-proof In contrast, the lowest cyst concentrations in the region off Luzon are unlikely effected by transport processes since the sediments consist of fine clayey silts and silty clays (Figure 4). Another important parameter that may affect the dinoflagellate cyst preservation in sediments is the high oxygen concentrations in bottom waters (e.g., Dale, 1976; Versteegh and Zonneveld, 2002; Zonneveld et al., 2007). Degradation-sensitive species could be oxidized during transport and deposition processes, especially when cysts are transported over large distances and

of

deposited at greater depths (e.g., Zonneveld et al., 1997). The water depth in the western region

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off Luzon is from ~2500 m to ~4000 m. Dissolved oxygen concentrations vary at different

-p

depths: higher oxygen above 600–700 m (e.g., ~3–3.5 ml l-1 at 140 m), lower oxygen between 700 and 1,500 m (e.g., ~2 ml l-1 at 1000 m) and higher oxygen again below 1,500 m (e.g., ~2.4–

re

2.6 ml l-1 at 2000–3000 m) (Qu 2002). Cyst loss due to oxidation might be a reason for very low

lP

cyst concentrations in this region as well as in the region off Taiwan at site 12 where the water

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depth is ~3000 m. The absence of an upwelling signal off Taiwan in the cyst record would be worth investigating further when more data on plankton and export processes become available.

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Heterotrophic dinoflagellates are mostly influenced by the distribution of their preferred

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prey (e.g., diatoms) (e.g., Jacobson and Anderson, 1986), whereas the distribution of autotrophic taxa depends on the availability of light and dissolved nutrients (e.g., Dale, 1996). Many studies report that active upwelling or nutrient-rich regions are characterized by cyst assemblages dominated by the heterotrophic taxa (e.g., Wall et al., 1977; Harland, 1983; Dale, 1996; Zonneveld and Brummer, 2000; Zonneveld et al., 2001; Dale et al., 2002; Fujii and Matsuoka, 2006; Radi et al., 2007; Pospelova et al., 2008, 2010; Price and Pospelova, 2011; Bringué et al., 2013, 2014; Zonneveld et al., 2013). Thus, the proportion of heterotrophic taxa in the cyst assemblages has been suggested as an indicator of nutrient availability associated with the

25

Journal Pre-proof presence of upwelling zones, increasing shore proximity or anthropogenic activity (e.g., Wall et al., 1977; Harland et al., 1983; Dale, 1996; Mudie and Rochon, 2001; Pospelova et al., 2004). Our study shows that the concentrations of cysts produced by heterotrophic dinoflagellates is similar to the total cyst concentrations in general, with the highest values found on the southern slope region off Borneo (Figure 6c). The highest percentages of heterotrophic taxa are in the regions off Borneo and Taiwan, and are likely associated with the upwelling in the SCS. The

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upwelling off Borneo forms and becomes stronger in winter and year-round Taiwan Bank

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upwelling intensifies to a peak between December and March (e.g., Ndah et al., 2017). The

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winter upwelling off Borneo provides nutrients for phytoplankton blooms, but it is not as strong

re

as upwelling off Taiwan which occurs during the entire year (e.g., Yan et al., 2015). Some inconsistencies between the cyst concentrations and proportions of heterotrophic taxa might also

lP

be associated with plankton composition in response to nutrient levels, and that is reflected in the

na

ratios of heterotrophs to autotrophs (Figure 6b). Water column samples from the oligotrophic Mediterranean coast showed that the ratio of heterotroph to autotroph planktonic biomass

ur

declined rapidly as a response to nutrient input (Duarte et al., 2006). A study on sediment traps

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of the SCS also showed that the ratios of heterotrophic to autotrophic dinoflagellate cysts declined when concentrations of the total cysts increased in summer seasons because of the greater amplitude of increases in autotrophs than in heterotrophic taxa (Li et al., 2018). This study shows that the concentrations of autotrophic taxa in the western and the northern regions (>250 cysts g-1 ) are much higher than those in the eastern and the southern regions (<100 cysts g1

) (Figure 6d), whereas the concentrations of heterotrophic taxa have concentrations > 250 cysts

g-1 only in the regions off Borneo and southern Vietnam (Figure 6c). In general, upwelling in the northern SCS is much more pronounced and stronger than in the southern SCS (e.g., Ndah et al.,

26

Journal Pre-proof 2016). The upwelling off southern Vietnam, Hainan, and South China is developed and becomes stronger in summer, whereas the upwelling off Borneo, Luzon and southern Taiwan is developed in winter. At the same time, much greater river inputs in summer also increase nutrients in the northern and the western SCS, more than in the southern and the eastern SCS (e.g., Zhao, 1990; Yin et al., 2004; Kao and Milliman, 2008; Wang et al., 2009; Ogston et al., 2017). Therefore, lower heterotrophic to autotrophic ratios may be related to greater nutrient inputs in the northern

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and the western SCS (Figure 6b).

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5.3. Dinoflagellate cysts associated with specific oceanographic parameters

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5.3.1. Dinoflagellate cysts associated with SST and SSS

Many studies of spatial distributions of dinoflagellate cysts in surface sediments have

lP

demonstrated that SST is one of the most important factors governing cyst distributions (e.g.,

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Harland, 1983; Dale, 1996; de Vernal et al., 2001, 2005; Radi and de Vernal, 2004; Radi et al., 2007; Pospelova et al., 2005, 2008; Limoges et al., 2010, Zonneveld et al., 2013). Our study

ur

shows that SST-Jan (P = 0.002) is positively and significantly correlated with the first axis of

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CCA, and SST-Jul (P = 0.028) is another significant parameter (Figure 7). The samples with the most positive scores of the first CCA axis are the sites in the southern slope-deep basin off Borneo, Luzon and the south offshore of Taiwan where SST-Jan is high (up to 27.8 °C), whereas the most negative scores are for the sites near the northern coast and in the northern slope-deep basin where low SSTs in January were observed (Figures 8a). Increased concentrations of Brigantedinium spp., Stelladinium reidii, Selenopemphix nephroides and Spiniferites bentorii are positively related to the first axis of CCA and they could be linked to warmer water conditions (Figure 7). Winter upwelling occurs in these warm water areas (Figure 3a) and nutrients are more

27

Journal Pre-proof abundant in winters than in summers. The highest concentrations of Brigantedinium spp., Selenopemphix nephroides and Stelladinium reidii (Figures 6e, 6n and 6o) were observed in the region off Borneo where diatom abundances (both in water and sediments) are the highest and can reach values of ~6–8 x 107 cells l-1 and ~6–8 x 106 cells g-1 , respectively (Lu et al., 2006). Previous studies have found that Brigantedinium spp. abundances were notably correlated with high abundances of diatoms due to increased nutrients as a result of upwelling (e.g., Fujii and

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Matsuoka, 2006; Pospelova et al., 2008, 2010; Price and Pospelova, 2011, Bringué et al., 2013).

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In contrast, Selenopemphix undulata, Spiniferites hyperacanthus, Spiniferites mirabilis,

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Spiniferites ramosus and Operculodinium longispinigerum are negatively correlated with SST-

re

Jan and are likely related to cooler waters (Figure 7). The result that Selenopemphix undulata has the most negative scores with SSTs in our study is consistent with other studies where

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Selenopemphix undulata was found to be most abundant in temperate cold waters in the Pacific

na

Ocean (e.g., Pospelova et al., 2006, 2008, 2015; Verleye et al., 2011). The highest concentrations of Selenopemphix undulata, Spiniferites hyperacanthus, Spiniferites mirabilis, Spiniferites

ur

ramosus and Operculodinium longispinigerum were observed off southern Vietnam, Hainan, and

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South China near summer upwelling zones or in shelf-break areas greatly influenced by internal waves and mixing (Figures 3b, 6J-6l and 6x). Dapsilidinium pastielsii was reported as a living fossil in the Indo-Pacific warm pool (Mertens et al., 2014). It was widespread during the Miocene when the climate was much warmer than the present (e.g., Tong et al., 2009; Merterns et al., 2014). Li et al. (2017) reported Dapsilidinium pastielsii in the SCS in high abundances at ~7000–6000 cal yr BP when air temperatures and SSTs were high and/or the Kuroshio Current intensified. In this study, for the first time, Dapsilidinium pastielsii was found in surface sediments from the SCS. Dapsilidinium

28

Journal Pre-proof pastielsii occurs only at the sites 19, 35 and 41 where water depth varies from ~170 m to ~1320 m, SST-Jan from 23°C to 25°C and SST-Jul is around 30°C (Figures 3 and 6ae, Table 1). Based on fossil occurrences of Dapsilidinium pastielsii in northwestern and central Italy, Zevenboom et al. (1994) suggested that this species is neritic and thermophilic. Live cysts were also discovered in Shioya Bay (Okinawa, Japan), Koror (Palau), Ambon (Indonesia), Masinloc (Philippines), and the East Vietnam Sea (Vietnam) where SSTs in summer are > 27°C (Mertens et al., 2014). Our

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findings indicate that Dapsilidinium pastielsii could be found under higher salinity conditions

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than it was originally suggested since the sites where we report Dapsilidinium pastielsii (Figure

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3c) have high SSS-Jan (~33) due to a strong Kuroshio Current Intrusion. Thus, higher SSSs

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might be another important factor for the presence of Dapsilidinium pastielsii when SSTs are high. Interestingly, no Dapsilidinium pastielsii cysts were found in the region off Borneo where

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lP

SST is high but PP is also one of the highest in the region.

5.3.2. Deep-sea dinoflagellate cysts

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CCA results show that Impagidinium, Nematosphaeropsis labyrinthus, and Polysphaeridium

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zoharyi are associated with the positive values of the second CCA axis of which water depth is a positive significant parameter (Figure 7a). Impagidinium aculeatum has the highest score and cysts of Lejeunecysta sabrina have the most negative scores (Figure 7a). The samples with the most positive scores are from the northern slope-basin of the SCS where SST-Jul and water depth are higher (Figures 7b, 8b and 8c). The concentrations and the percentages of total Impagidinium, consisting of Impagidinium spp., Impagidinium aculeatum, Impagidinium paradoxum, and Impagidinium patulum, as well as Polysphaeridium zoharyi, display the highest values in the slope-basin of the SCS (Figures 6y, 6z, 6aa, 6ab and 6ac). The highest values of

29

Journal Pre-proof concentrations and percentages of Nematosphaeropsis labyrinthus are in the southern deep basin (Figure 6ad), but the abundances, in general, are not very high (0–3%; 0–10 cysts g-1 ). After analyzing dinoflagellate cyst data from 2405 globally distributed surface sediment samples, Zonneveld et al. (2013) stated that Impagidinium strialatum, Impagidinium patulum, and Impagidinium paradoxum are restricted to fully marine environments. These species are considered to indicate open oceanic, fully- marine, low primary productivity settings with well-

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ventilated bottom waters (e.g., Zonneveld et al., 2013). Impagidinium aculeatum is also a marine

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species (e.g., Dale, 1996; Rochon et al., 1999; de Vernal, 2001; Marret and Zonneveld, 2003;

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Pospelova et al., 2008; Zonneveld et al., 2013; Limoges et al., 2014). Polysphaeridium zoharyi is

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commonly observed in coastal subtropical to tropical regions that may have high productivity (Azanza et al., 2004; Zonneveld et al., 2013; Price et al., 2016, 2018). Its maximum (~ 70%) was

lP

observed in the Gulf of Mexico (e.g., Marret and Zonneveld, 2003, Limoges et al., 2013, 2015)

na

and off SW Mexico (Limoges et al., 2010). However, it occurs in very low abundances (relative abundances < ~5%, concentrations < ~35 cysts g-1 ) in the SCS and in the north coastal waters of

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Sabah in Malaysia (Figure 6) (e.g., Furio et al., 2006). Furio et al. (2006) suggested that strong

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waves and well-developed water circulations transported or washed away Polysphaeridium zoharyi elsewhere in its neighboring coastal waters since they found its abundances to be very low in surface sediments off the coasts of Sabah in Malaysia although their theca cells occurred frequently in harmful algal blooms in the overlying waters. Similarly, internal waves at the shelfbreak zone where the highest abundances were observed might be the transport force in our records (Figure 6y). Nematosphaeropsis labyrinthus is considered a cosmopolitan species with a broad temperature tolerance (e.g., Zonneveld et al., 2013). However, it was also reported to be

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Journal Pre-proof associated with oceanic and low productivity sites in the northeastern Pacific Ocean (e.g., Pospelova et al., 2008).

5.3.3. Dinoflagellate cysts associated with high chl-a concentrations Chl-a-Jul is indicated to be the most important parameter for the distributions of Lejeunecysta sabrina, Quinquecuspis concreta and cysts of Protoperidinium spp. Lejeunecysta

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sabrina has the most negative score on the second CCA axis (Figure 7a). Figure 8d shows that

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the sites with high negative scores of the second CCA axis are in the coast-shelf regions where

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chl-a concentrations are high. Sites with high positive scores are observed in the northern slope-

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deep basin where chl-a concentrations are low (Figure 8d). Chl-a concentrations in the SCS are generally higher along the coast, rapidly decrease offshore, and become very low in the deep

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basin (Figure 8d). Influenced by the seasonal monsoons, there are clear chl-a concentration

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differences between the eastern and the western coast of the SCS. Chl-a concentrations along the western coast increase in summer and decline in winter, whereas this trend is reversed along the

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eastern coast (Kuo et al., 2009). Chl-a concentrations generally represent the level of

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phytoplankton biomass and high concentrations are commonly associated with high primary productivity (e.g., Tang et al., 2004). In this study, the species that positively correlate with chl-a concentrations are produced by heterotrophic dinoflagellate taxa. However, they are not the dominant species in the cyst assemblages. Concentrations and relative abundances of these taxa are all much lower than those of Brigantedinium spp., the most dominant group among heterotrophic taxa in the SCS (Figures 6e and 6m). Abundances of Brigantedinium spp. have been used as indicators of primary productivity (e.g., Zonneveld and Brummer, 2000; Marret and Zonneveld, 2003; Pospelova et al., 2008, 2015; Radi and de Vernal, 2008; Verleye and Louwye,

31

Journal Pre-proof 2010; Bringué et al., 2013; Price et al., 2013; de Vernal et al., 2013, Bringué et al., 2018). However, our results show that an assemblage dominated by cysts of Protoperidinium spp., Lejeunecysta sabrina and Quinquecuspis concreta rather than Brigantedinium spp. has a closer positive relationship with chl-a concentrations in the SCS (Figure 7). This might be associated with a non- linear relationship between chl-a concentrations and PP which is worth investigating

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in the future.

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6. Conclusions

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Geographical distributions of dinoflagellate cysts were investigated in the SCS to determine

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the influence of local environmental parameters on cyst contributions and to identify taxa indicative of modern environmental conditions. The most common heterotrophic taxa in the SCS

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are Brigantedinium spp., Echinidinium spp., Selenopemphix nephroides, Selenopemphix quanta,

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Stelladinium reidii, Trinovantedinium applanatum, and cysts of Protoperidinium spp. The most abundant cysts of autotrophic dinoflagellates are Impagidinium, Lingulodinium, Operculodinium,

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Spiniferites and less abundant are Nematosphaeropsis labyrinthus and Polysphaeridium zoharyi.

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In general, the western SCS has higher total cyst concentrations than the eastern region. The higher total cyst concentrations occur mainly in the regions off southern Vietnam, Borneo (southern slope of SCS), Hainan and South China where active upwelling zones exist or internal waves occur along the shelf-break zones. The highest concentrations of total dinoflagellate cysts and autotrophic taxa occur in the nearshore sites of southern Vietnam, and the lowest concentrations are in the deeper regions off Luzon and Taiwan. The highest abundances of heterotrophic taxa occur on the southern slope off Borneo. The ratios of heterotrophic to autotrophic taxa have an opposite distributional pattern to the total cyst concentrations, which

32

Journal Pre-proof might reflect much greater increases in autotrophic taxa abundances than in heterotrophic taxa when nutrients increase. Brigantedinium spp., Selenopemphix nephroides, and Selenopemphix reidii have similar distributional patterns, with the highest abundances in the region off Borneo. The highest abundances of Trinovantedinium applanatum, Votadinium spp., cysts of Protoperidinium spp., and Quinquecuspis concreta are in the region off southern Vietnam. High abundances of total

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Impagidinium, Impagidinium aculeatum, Impagidinium paradoxum, Impagidinium patulum,

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Nematosphaeropsis labyrinthus, and Polysphaeridium zoharyi all appear in the slope-deep basin,

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especially in the northern slope-basin influenced by the Kuroshio Current. Most of the other taxa

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have their highest abundances in the northern slope off South China, Hainan, and southern Vietnam, whereas the lowest abundances are recorded in the regions off Borneo and Taiwan.

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Dapsilidinium pastielsii is rare and is found at sites in the north-western region of the SCS that

Jan.

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are influenced by the Kuroshio Current in winter and characterized by high SSSs and low SST-

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SST-Jan, WD, Chl-a-Jul and SST-Jul are the four most important factors in modern

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dinoflagellate cyst distributions in the SCS. Brigantedinium spp., Selenopemphix nephroides and Selenopemphix reidii are positively correlated with SST-Jan. High abundances of these taxa are likely associated with warmer sea-surface conditions near winter upwelling zones. In contrast, high abundances of heterotrophic Selenopemphix undulata and autotrophic Spiniferites hyperacanthus and Operculodinium longispinigerum are linked to cooler sea-surface waters in summer and near upwelling zones. As expected, autotrophic Impagidinium spp., Impagidinium patulum, Impagidinium paradoxum, Impagidinium aculeatum, and Nematosphaeropsis labyrinthus are found in the

33

Journal Pre-proof open-ocean environments, at sites characterized by deep waters and away from coastlines or nutrient sources. The highest abundances are documented in the northern SCS that is influenced by the Kuroshio Current. Cysts of Protoperidinium spp., Lejeunecysta sabrina, Quinquecuspis concreta, and Selenopemphix quanta are associated with higher chl-a concentrations and are found in high primary productivity regions. This comprehensive study of modern dinoflagellate cyst distributions and environmental

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factors influencing dinoflagellate cysts in the SCS provides insights into the ecology of

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individual dinoflagellate cyst taxa and essential information for future paleoceanographic studies

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using dinoflagellate cysts in the region. Our data fill a gap in the existing global dinoflagellates

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database and provide a valuable addition to the database for future quantitative reconstructions of

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oceanographic conditions.

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Acknowledgements

The Natural Sciences and Engineering Research Council of Canada (NSERC) CGS D3

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fellowship (CGSD3-475098-2015) and Montalbano scholarship provided partial funding for this

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research to Z. Li. This work was also funded by NSERC through a Discovery grant (RGPIN/6388-2015) to V. Pospelova. She is the Hanse-Wissenschaftskolleg (HWK) senior research fellow in marine and climate research at the Institute for Advanced Study (Germany). Editor- in-chief R. Jordan, guest editor N. Van Nieuwenhove and two anonymous reviewers are acknowledged for their very constructive suggestions and comments.

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List of tables and figures Table 1. Geographical coordinates and sediment types of studied surface sediment samples, water depth (WD), distance to the coastline (DC), chl-a concentrations, sea-surface temperature

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Journal Pre-proof (SST) and salinity (SSS), the number of counted dinoflagellate cysts and Lycopodium grains per sample, as well as dry weight of samples used for this study and by Kawamura (PhD thesis, 2002; 2004). Environment data are from http://marine.copernicus.eu. Note: In this study, one Lycopodium clavatum tablet (9666 grains per tablet) was added to each sample, except for two tablets into samples marked with "*". A total of 12,542 grains of Lycopodium clavatum spores were added to each sample from

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Kawamura (2002; 2004).

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Data of chl-a concentrations, SST and SSS are respectively the averages of January, July and

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Annual from 1997 to 2016.

Table 2. List of dinoflagellate cyst taxa identified in this study. The cyst-theca equivalents are

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based on McMinn (1991), Kokinos and Anderson (1995), Head (1996), Zonneveld (1997),

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Zonneveld and Jurkschat (1999), Esper and Zonneveld (2002), Pospelova and Head (2002), Matsuoka et al. (2009), Pospelova and Kim (2010), Verleye et al. (2011), Mertens et al. (2014,

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2017, 2018), Zonneveld and Pospelova (2015), and Gurdebeke et al., (2019).

Table 3. Names of dinoflagellate cyst taxa in this study, Kawamura (2002, 2004) and in the combined dataset. Note: the name of taxon that a species was transferred or grouped to was listed in [ ]. Calcareous cysts and others, which were included in dinoflagellate cysts in the dataset of Kawamura (2002, 2004), were excluded in the combined datasets.

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Journal Pre-proof Figure 1. Map of the study area showing sampling sites and bathymetry of the South China Sea (modified from Wang et al., 2008; Li et al., 2017). The red triangles on the map indicate locations of samples from this study. The green squares mark locations of samples from previously published data of Kawamura (2002, 2004).

Figure 2. Wind velocities in January (a) and July (b), and sea water velocities in January (c) and

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July (d). White arrow lines are currents directions (modified from http://marine.copernicus.eu

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and Fang et al., 1998).

sea-surface

salinity

(SSS)

in

(c)

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Figure 3. Sea-surface temperature (SST) of the South China Sea in (a) January and (b) July and January

and

(d)

July

(modified

from

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http://marine.copernicus.eu). Circles with numbers in Figure 3a and 3b show upwelling zones

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developing: during winter off Borneo (1), Luzon (2) and Taiwan (3); year-round on Taiwan

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Bank (4) and during summer off South China (5–6), Hainan (7) and southern Vietnam (8–9).

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Figure 4. Total cyst concentrations (cysts g-1 ) and relative abundances of selected cyst taxa ( contributing >1%) in surface sediment samples grouped by regions. On the right, water depth and sediment types are shown for each site (C-Clay, Slt-Silt, FS-Fine Sand, and CS-Coarse Sand). Heterotrophic taxa are shown in green and autotrophic taxa are in blue. The black line separates samples 1–42 (this study) from samples 43–76 (Kawamura (2002, 2004)). Samples with counts < 100 are not included in relative abundance calculations.

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Journal Pre-proof Figure 5. Concentrations (cysts g-1 ) of selected dinoflagellate cyst taxa in surface sediment samples that were grouped by region. Heterotrophic taxa are shown in green and autotrophic taxa are in blue. The black line separates samples 1–42 (this study) from samples 43–76 (Kawamura (2002, 2004). Samples with the total cyst counts < 100 are also included.

Figure 6. Contour maps of the total cyst concentrations (cysts g-1 ), the ratios of heterotrophic to

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autotrophic taxa, concentrations and relative abundances of autotrophic taxa, heterotrophic taxa

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and selected heterotrophic taxa from the combined dataset. Samples with < 100 counted cysts are

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not shown on the maps with percentages and the ratio of heterotrophic to autotrophic. Circles

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with numbers correspond to upwelling regions in Figure 3a and 3b.

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Figure 7. Canonical Correspondence Analysis (CCA) performed on the dinoflagellate cyst

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concentrations (cysts g-1 ) and environmental parameters. SST-Jan: mean sea-surface temperature in January; SST-Jul: mean sea-surface temperature in July; SSS-Jan: mean sea-surface salinity in

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January; SSS-Jul: mean sea-surface salinity in July; Chl-a-Jan: mean chl-a concentrations in

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January; Chl-a-Jul: mean chl-a concentrations in July; PP: primary productivity; WD: water depth; DC: distance to the coastline. All data of SST, SSS and chl-a concentrations are from 1997 to 2016. Ordination diagram showing species scores (7a) and sample scores (7b). Marginal effects, conditional effects and summary of CCA axes statistics are shown as well. P-values <0.05 are statistically significant and highlighted in bold. Lambda (A) is the variation explained by each environmental variable, considered independently (marginal effect), or considered after all variables already incorporated in the model (conditional effect). Solid arrows represent forward-selected variables and dashed arrows represent non-significant environmental variables.

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Figure 8. The distributions of CCA 1 scores for each sample shown on the map of (a) SST in January (SST-Jan), and CCA 2 scores on the maps of (b) SST in July (SST-Jul), (c) Water depth, and (d) Chl-a concentrations in July (Chl-a-Jul). The scales of SST color bars are different

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between (a) and (b).

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Plate I. 1. Dapsilidinium pastielsii, UVic201711, 2. Impagidinium aculeatum, UVic2017-20, 3a,

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3b. Impagidinium patulum, UVic2017-23, 4a, 4b. Impagidinium sphaericum, UVic2017-13, 5a,

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5b. Impagidinium cf. sphaericum, UVic2017-19, 6a, 6b. Impagidinium paradoxum UVic201716, 7. Impagidinium strialatum, UVic2017-1 slide 1, 8. Lingulodinium hemicystum, UVic2017-

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13, 9. Lingulodinium sp. A, UVic2017-2, 10. Nematosphaeropsis labyrinthus, UVic2017-64, 11.

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Operculodinium centrocarpum sensu Wall and Dale 1966, UVic2017-1 slide 1. 12–13. Atlanticodinium striaticonulum Head and Mantilla-Duran (Operculodinium sp. A of Vink 2000),

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12: UVic2017-9, 13: UVic2017-26, 14a, 14b. Cyst of Pentaplacodinium saltonense, UVic2017-

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11, 15. Operculodinium sp. UVic2017-9. Scale bars = 10 μm.

Plate II. 1a, 1b. Operculodinium longispinigerum, UVic2017-13, 2–4. Polysphaeridium zoharyi, 2：UVic2017-65, 3：UVic2017-1 slide 1, 4：UVic2017-5, 5. Spiniferites bentorii, UVic2017-2, 6a, 6b, 7a, 7b. Spiniferites hyperacanthus, 6a, 6b：UVic2017-1 slide 1, 7a, 7b：UVic2017-26, 8– 9a, 9b. Spiniferites mirabilis, 8：UVic2017-1 slide 1, 9a, 9b：UVic2017-52, 10a, 10b. Spiniferites pachydermus, UVic2017-62, 11. Spiniferites pacificus, UVic2017-10, 12–13.

60

Journal Pre-proof Spiniferites ramosus, 12：UVIc2017-1 slide 1, 13a, 13b：UVic2017-25, 14. Tuberculodinium vancampoae, UVic 2017-1 slide 1. Scale bars = 10 μm.

Plate III. 1. Brigantedinium cariacoense, UVic2017-5, 2–3. Brigantedinium spp., 2：UVic201711, 3：UVic2017-1 slide 1, 4. Brigantedinium-type A, UVic2017-32, 5a, 5b. Cryodinium cf. meridianum, UVic2017-20, 6. Dubridinium cavatum, UVic2017-27, 7. Dubridinium sp.,

of

UVic2017-5, 8. Echinidinium aculeatum, UVic2017-2, 9. Echinidinium sp., UVic2017-2. 10.

ro

?Leipokatium invisitatum, UVic2017-53, 11. Votadinium ?pontifossatum, UVic2017-49, 12.

-p

Votadinium elongatum, UVic2017-11, 13–14. Cysts of Protoperidinium spp., 13：UVic2017-50,

re

14：UVic2017-26, 15. Selenopemphix nephroides, UVic2017-53, 16. Selenopemphix quanta, UVic2017-23 slide 1, 17. Selenopemphix tholus, UVic2017-50, 18. Stelladinium reidii,

Jo

ur

na

lP

UVic2017-2, 19. Trinovantedinium applanatum, UVic2017-25. Scale bars = 10 µm.

61

Journal Pre-proof Table 1.

Site

Sample

Latitude

No.

Code

(N)

Longitude Collection (E)

date

1 2 3

OR1-0455-15-B OR1-0455-16-B OR1-0455-17-B

13°30.30' 13°55.68' 14°20.76'

118°56.64' 118°39.84' 118°45.18'

05/18/2016 05/18/2016 05/18/2016

4 5 6 7

OR1-0455-19-B OR1-0455-21-B OR1-0455-10-B OR1-0455-9-B

15°05.28' 15°33.84' 14°18.84' 14°34.74'

118°26.70' 118°10.80' 119°25.08' 119°38.10'

8 9 10

OR1-0455-7-B OR1-0455-6-B OR1-0455-2-B

14°45.78' 14°54.60' 15°57.48'

11 12 13

OR1-0455-1-B 09-E401 OR1-0216-1-B

14 15 16

Sediment type

WD DC Chl-a concentr ations (mg m -3)

SST (°C)

SSS

Annual

Clayey silt Silty clay Silt

3558 131 3447 180 4060 155

0.16 0.16 0.15

0.11 0.11 0.10

0.13 0.12 0.12

27.4 27.4 27.4

29.4 29.4 29.4

28.8 28.8 28.8

33.1 33.1 33.1

33.1 33.1 33.1

33.1 33.1 33.2

4 0 0

05/18/2016 05/18/2016 05/18/2016 05/18/2016

Silty clay Clayey silt Silt Silt

3943 3681 2481 2602

158 174 92 53

0.15 0.15 0.15 0.15

0.10 0.09 0.11 0.11

0.12 0.12 0.13 0.13

27.2 26.8 27.4 27.3

29.5 29.6 29.5 29.6

28.8 28.7 28.8 28.8

33.1 33.2 33.2 33.2

33.2 33.2 33.1 33.1

33.2 33.2 33.1 33.1

0 0 4 14

119°38.34' 119°32.28' 118°53.04'

05/18/2016 05/18/2016 05/18/2016

Silty clay Fine sand Silty clay

2592 46 2509 55 3706 92

0.14 0.14 0.15

0.11 0.10 0.09

0.12 0.12 0.12

27.3 27.3 26.6

29.6 29.6 29.7

28.8 28.8 28.7

33.2 33.2 33.2

33.1 33.2 33.2

33.1 33.1 33.2

8 5 11

16°14.16' 21°29.78' 21°49.98'

118°55.62' 120°04.48' 121°01.98'

05/18/2016 09/17/2009 05/18/2016

Silty clay Sandy clay Clay

3860 88 3059 85 1310 20

0.15 0.28 0.30

0.09 0.10 0.10

0.12 0.16 0.17

26.5 25.0 24.9

29.8 29.6 29.7

28.6 27.4 27.3

33.3 34.4 34.4

33.2 33.6 33.6

33.2 34.0 34.0

5 25 146

OR1-0182-3-B OR1-0299-1-B-1 OR1-0299-2-B-2

21°58.62' 22°27.72' 22°29.90'

120°54.72' 120°22.50' 120°15.80'

05/18/2016 05/18/2016 05/18/2016

Clay Silty clay Silty clay

373 24 138

5 3 13

0.27 0.77 0.33

0.37 1.62 0.41

0.32 1.34 0.39

24.6 23.0 23.8

29.6 29.8 29.8

27.2 26.5 26.8

34.4 34.2 34.3

32.8 28.9 31.5

33.6 32.2 33.0

87 117 79

17 18 19

08-CF2 08-E605 08-CF10

22°07.00' 19°59.30' 20°11.14'

119°17.26' 117°32.36' 116°28.51'

2008 2008 2008

Silty clay Clayey silt Sand

1320 113 2346 402 863 294

0.30 0.35 0.32

0.13 0.12 0.11

0.18 0.18 0.18

24.6 24.0 23.7

29.6 29.5 29.5

27.2 27.0 26.9

34.4 34.0 34.1

33.5 33.6 33.5

33.9 33.4 33.8

141 10 85

20 21 22

09-E108 OR1-0311-68-B OR1-0311-56-B

21°17.75' 21°28.20' 22°45.00'

116°24.16' 116°39.78' 117°06.12'

09/19/2009 05/18/2016 05/18/2016

Medium-coarse sand Coarse sand Fine sand

318 172 325 163 41 65

0.37 0.37 0.86

0.22 0.23 0.93

0.22 0.24 0.63

23.6 23.6 19.6

29.4 29.4 28.6

26.5 26.5 24.7

34.2 34.2 33.4

33.5 33.5 30.7

33.8 33.8 32.6

18 13 11

23 24 25

OR1-0311-90-B OR1-0311-80-B 79-48

21°34.14' 21°31.92' 19°58.00'

114°32.46' 115°41.04' 115°00.00'

05/18/2016 05/18/2016 2008

Silty clay Clayey silt Silty clay

72 94 113 127 1100 259

0.52 0.39 0.37

0.42 0.25 0.13

0.42 0.27 0.19

21.7 22.8 23.5

29.1 29.4 29.5

25.7 26.1 26.8

33.7 34.1 34.1

33.2 33.4 33.6

33.4 33.7 33.8

344 160 322

26 27 28

08-E702 08-E525 08-E524

19°30.24' 19°24.02' 19°39.84'

115°31.01' 114°35.83' 112°33.41'

2008 2008 2008

Clayey silt Clayey silt Medium-coarse sand

2365 311 1190 310 150 161

0.30 0.32 0.32

0.11 0.11 0.11

0.17 0.17 0.18

23.6 23.6 23.6

29.5 29.5 29.4

26.9 26.9 26.8

34.1 34.1 34.0

33.6 33.6 33.5

33.8 33.7 33.7

31 77 282

29 30 31

D15-3 08-E501 D21-3

20°42.00' 18°51.78' 18°09.85'

110°51.00' 110°40.47' 110°14.43'

2008 2008 2008

Silty clay Clayey silt Sandy clay

34 16 31

2.41 0.46 0.34

1.33 0.32 0.17

1.77 0.42 0.27

18.9 22.8 23.5

29.5 27.8 29.3

25.0 26.1 26.9

32.0 33.7 33.8

32.5 33.4 33.2

31.6 33.4 33.5

98 112 57

32 33 34

D22a-1 09-E605 08-E425(CF6)

18°01.75' 17°23.37' 18°04.30'

109°29.91' 110°10.83' 110°58.23'

2008 09/06/2009 2008

Silty clay Silty clay Silty clay

43 16 768 105 1211 89

0.60 0.25 0.27

0.24 0.13 0.13

0.40 0.16 0.17

23.5 24.2 24.1

29.2 29.7 29.4

26.8 27.2 27.1

33.6 33.8 33.9

33.1 33.4 33.4

33.3 33.5 33.6

225 329 271

35 36 37

08-E504 09-KJ16 09-KJ14

18°38.21' 17°59.20' 18°03.57'

111°14.48' 111°59.30' 113°01.82'

2008 06/15/2009 06/15/2009

Clayey silt Silty clay Silty clay

168 77 2310 107 2290 136

0.26 0.25 0.24

0.13 0.11 0.11

0.17 0.15 0.15

23.9 24.2 24.1

29.4 29.5 29.5

27.0 27.2 27.2

33.9 33.9 34.0

33.4 33.5 33.5

33.6 33.6 33.6

324 376 38

38 39

09-E420 09-KJ21

18°01.15' 17°31.13'

113°31.78' 113°01.32'

09/12/2009 05/20/2009

Clayey silt Sandy mud

1929 159 1466 83

0.24 0.22

0.11 0.11

0.14 0.14

24.0 24.3

29.5 29.6

27.2 27.4

34.0 33.9

33.4 33.4

33.6 33.5

47 35

(to continue) Site Sample No. Code

Latitude (N)

Longitude Collection (E) date

40

09-Y01

17°04.74'

111°45.64'

09/07/2009

Silty clay

1125 43

0.22

0.12

0.15

24.7

29.6

27.5

33.2

32.8

32.9

166

41 42 43

09-Y07 09-KJ28 17954-1

16°24.28' 13°58.50' 14°45.50'

112°10.39' 113°02.35' 111°31.60'

09/06/2009 05/21/2009 1997

Clayey silt Sandy mud Clay

955 16 2460 235 1517 139

0.21 0.16 0.16

0.12 0.13 0.12

0.19 0.13 0.14

24.9 26.2 25.7

29.7 29.0 29.5

27.8 28.1 28.0

33.0 32.9 32.9

32.8 33.3 33.2

32.9 33.0 33.0

129 23 136

44 45 46

17950-1 17952-1 17949-1

16°05.60' 16°40.00' 17°20.90'

112°53.80' 114°28.40' 115°10.10'

1997 1997 1997

Sandy silt Clay Clay

1868 50 2340 260 2195 332

0.17 0.19 0.23

0.11 0.10 0.10

0.13 0.14 0.14

25.1 25.1 24.5

29.5 29.6 29.6

27.8 27.8 27.5

33.0 33.3 33.4

32.8 33.1 32.9

32.9 33.1 33.0

193 121 132

47 48 49

17945-1 17942-1 17939-1

18°07.60' 19°20.00' 19°58.20'

113°46.60' 113°12.10' 117°27.30'

1997 1997 1997

Clay Sandy silt Clay

2404 241 329 231 2473 344

0.27 0.32 0.35

0.11 0.11 0.13

0.15 0.18 0.18

24.0 23.7 23.9

29.5 29.5 29.5

27.2 26.9 27.0

33.3 33.2 33.5

32.9 32.8 33.0

33.1 33.0 33.1

98 243 249

50 51 52

17925-1 17926-1 17927-1

19°51.20' 19°00.00' 17°15.00'

119°02.80' 118°44.00' 119°27.20'

1997 1997 1997

Clay Clay Clay

2980 218 3761 199 2800 101

0.42 0.37 0.16

0.10 0.09 0.10

0.19 0.18 0.12

24.6 24.4 26.3

29.6 29.6 29.9

27.4 27.5 28.5

33.2 33.5 32.7

33.1 33.1 33.0

33.1 33.2 32.9

56 79 70

53

17958-1

11°37.10'

115°04.90'

1997

Clay

2581 48

0.16

0.11

0.12

27.7

29.1

28.7

32.7

33.0

32.9

112

ro

-p

re

lP

na

Jo

ur

Sediment type

of

July

25 95 50

Januar y July Annual Januar y

Counted number of:

(m) (km) Januar y

WD DC Chl-a concentr ations(mg m -3) SST (°C) (m) (km) Januar y July Annual Januar y July Annual

SSS Januar y

July Annual

July Annual

Dinoflagellate cysts

Lyco

Counted number of: Dinoflagellate cysts Lyco

62

Journal Pre-proof 17959-1 17962-1 17965-1

11°08.30' 07°10.90' 06°09.40'

115°17.20' 112°04.90' 112°33.10'

1997 1997 1997

Clay Clay Silty clay

1957 37 1970 68 889 59

0.16 0.19 0.24

0.10 0.12 0.11

0.12 0.14 0.15

27.8 27.3 27.6

29.1 29.2 29.6

28.8 28.8 28.9

32.7 32.8 32.7

33.0 33.1 33.1

32.9 33.0 32.9

213 387 320

57 58 59

18300-1 18374-1 18381-1

04°21.77' 06°54.77' 07°29.86'

108°39.21' 107°39.91' 109°07.64'

1997 1997 1997

Clayey sand Silty sand Clayey silt

94 121 74 313 214 380

0.21 0.21 0.19

0.11 0.17 0.12

0.14 0.16 0.14

27.0 25.9 26.5

29.7 29.3 29.4

28.9 28.3 28.5

33.1 33.2 32.9

33.1 32.7 32.8

33.0 33.0 32.8

98 29 130

60 61 62

18384-1 18386-1 18392-1

07°46.33' 07°54.09' 09°37.08'

109°48.68' 110°07.85' 108°54.36'

1997 1997 1997

Clay Sandy silt Silty sand

829 464 380 386 116 163

0.20 0.24 0.25

0.13 0.13 0.17

0.14 0.15 0.21

26.6 26.7 25.6

29.2 29.1 29.1

28.5 28.5 28.0

32.9 32.9 32.8

32.8 33.0 32.6

32.8 32.9 32.7

266 66 130

63 64 65

18394-1 18395-1 18397-1

09°47.67' 09°59.22' 12°14.71'

109°10.88' 109°28.73' 109°19.91'

1997 1997 1997

Silty clay Clayey silt Silty clay

183 152 280 160 45 10

0.19 0.18 0.76

0.15 0.14 0.39

0.17 0.17 0.55

25.8 26.0 25.0

29.2 29.2 26.9

28.1 28.1 27.2

32.8 32.8 34.3

32.6 32.6 34.1

32.7 32.7 34.0

327 126 299

66 67 68

18401-1 18404-1 18405-1

13°30.12' 13°41.11' 14°14.90'

109°33.67' 109°27.02' 109°20.20'

1997 1997 1997

Clay Clayey sand Clay

134 169 129

28 20 15

0.30 0.60 0.63

0.19 0.20 0.20

0.27 0.39 0.41

24.6 24.5 24.4

28.9 28.6 28.6

27.5 27.3 27.2

32.9 32.9 33.0

33.0 33.0 33.3

33.0 33.0 33.0

206 61 267

69 70 71

18413-1 18412-1 18409-1

14°44.81' 15°12.18' 15°13.35'

109°17.61' 109°00.21' 109°00.74'

1997 1997 1997

Clayey silt sand & gravel Clayey silt sand & gravel Clay

52 58 40

23 8 7

0.47 1.36 1.18

0.16 0.23 0.21

0.33 0.74 0.67

24.4 24.0 24.0

29.2 28.6 28.7

27.3 27.0 27.0

33.0 33.2 33.2

33.3 33.2 33.2

33.0 33.2 33.2

40 88 264

72 73 74

18421-1 18408-1 18428-1

15°44.94' 15°41.21' 16°23.59'

108°53.33' 108°40.79' 109°25.04'

1997 1997 1997

Sandy silty clay Clay Sandy silt

83 35 117 40 197 126

0.58 1.36 0.25

0.17 0.21 0.14

0.40 0.79 0.17

24.0 23.8 24.3

29.3 29.1 30.0

27.2 27.0 27.4

33.7 33.7 33.2

33.0 33.0 33.0

33.3 33.3 33.0

22 253 224

75 76

18427-1 18426-1

16°28.55' 16°44.40'

109°11.47' 108°27.77'

1997 1997

Silty clay Sandy silt

115 100 93 63

0.25 0.50

24.3 23.8

30.0 29.7

27.4 27.1

33.2 33.2

33.0 32.9

33.0 33.0

123 135

ro

of

54 55 56

0.19 0.30

Jo

ur

na

lP

re

-p

0.13 0.16

63

Journal Pre-proof Table 2. Cyst species (paleontological name)

Dinoflagellate theca or affinity (biological name)

Autotrophic taxa

ro

of

?Gonyaulax sp. Indet. Unknow n Gonyaulax sp. indet. Alexandrium spp. Pentaplacodinium saltonense ? Unknow n Gonyaulax spp. Gonyaulax spp. Gonyaulax spp. Gonyaulax spp. Gonyaulax sp. indet. Gonyaulax spp. ?Lingulodinium polyedra Lingulodinium spp. Gonyaulax spinifera Protoceratium reticulatum ?Protoceratium reticulatum ?Protoceratium reticulatum Unknow n Unknow n Pyrodinium bahamense Gonyaulax digitales Gonyaulax spinifera complex? Gonyaulax spinifera complex Gonyaulax spinifera complex Gonyaulax spinifera complex Gonyaulax membranacea Gonyaulax spinifera complex Gonyaulax spinifera complex Gonyaulax ellegaardiae Gonyaulax spinifera complex Gonyaulax spinifera complex Pyrophacus steinii

Jo

Heterotrophic taxa

ur

na

lP

re

-p

Gonyaulacales Achomosphaera spp. Atlanticodinium striaticonulum (Operculodinium sp. A of Vink 2000) Bitectatodinium spongium Cyst of Alexandrium spp. Cyst of Pentaplacodinium saltonense Dapsilidinium pastielsii Impagidinium aculeatum Impagidinium paradoxum Impagidinium patulum Impagidinium sphaericum Impagidinium cf. sphaericum Impagidinium strialatum Impagidinium spp. Lingulodinium hemicystum (machaerophorum) Lingulodinium spp. Nematosphaeropsis labyrinthus Operculodinium centrocarpum sensu Wall and Dale 1966 Operculodinium cf. israelianum Operculodinium israelianum Operculodinium longispinigerum Operculodinium spp. Polysphaeridium zoharyi Spiniferites bentorii Spiniferites bulloideus Spiniferites delicatus Spiniferites hyperacanthus Spiniferites cf. ludhamensis Spiniferites membranaceus Spiniferites mirabilis Spiniferites pacificus Spiniferites pachydermus Spiniferites ramosus Spiniferites spp. Tuberculodinium vancampoae Peridiniales Cyst of Pentapharsodinium dalei

Peridiniales Brigantedinium cariacoense Brigantedinium irregulare Brigantedinium simplex Brigantedinium spp. Cryodinium cf. meridianum Cyst of Protoperidinium spp. Dubridinium caperatum Dubridinium cavatum Echinidinium aculeatum Echinidinium granulatum Echinidinium transparantum Echinidinium spp. Lejeunecysta sabrina Leipokatium invisitatum Quinquecuspis concreta Selenopemphix nephroides Selenopemphix quanta Selenopemphix tholus Selenopemphix undulata Stelladinium reidii Trinovantedinium applanatum Votadinium elongatum

Pentapharsodinium dalei

Protoperidinium avellanum Protoperidinium denticulatum Protoperidinium conicoides Protoperidinium spp. Protoperidinium spp. Protoperidinium spp. ?Preperidinium meunieri Diplopsalid group Diplopsalid or Protoperidinioid group Diplopsalid or Protoperidinioid group Diplopsalid or Protoperidinioid group Diplopsalid or Protoperidinioid group ?Protoperidinium leonis Unknow n Protoperidinium leonis Protoperidinium subinerme Protoperidinium conicum Protoperidinium spp. Unknow n Protoperidinium compressum Protoperidinium pentagonum Protoperidinium spp.

64

Journal Pre-proof Protoperidinium spp.

Jo

ur

na

lP

re

-p

ro

of

Votadinium spp.

65

Journal Pre-proof Table 3. Cyst taxa from this study

Cyst taxa in the com bined dataset

Autotrophic Achomosphaera spp. Alexandrium tamarensis [Cyst of Alexandrium spp.] Impagidinium aculeatum Impagidinium paradoxum Impagidinium patulum Impagidinium sphaericum [Impagidinium spp.] Impagidinium strialatum [Impagidinium spp.] Impagidinium spp. [Impagidinium spp.] Lingulodinium machaerophorum [L. hemicystum] Lingulodinium machaerophorum(short process) [L. hemicystum] Nematosphaeropsis labyrinthus Operculodinium centrocarpum Operculodinium crassum [Operculodinium spp.] Operculodinium israelianum [Operculodinium spp.] Operculodinium janduchenei [Operculodinium spp.] Operculodinium longispinigerum Polysphaeridium zoharyi Spiniferites bentorii Spiniferites bulloideus [Spinif erites spp.] Spiniferites delicatus [Spiniferites spp.] Spiniferites hyperacanthus Spiniferites membranaceus [Spiniferites mirabilis] Spiniferites mirablis Spiniferites ramosus Spiniferites spp. [Spiniferites spp.] Tuberculodinium vancampoae

Autotrophic Achomosphaera spp. Atlanticodinium striaticonulum [Operculodinium spp.] Bitectatodinium spongium Dapsilidinium pastielsii Impagidinium aculeatum Impagidinium pallidum [Impagidinium spp.] Impagidinium paradoxum Impagidinium patulum Impagidinium sphaericum [Impagidinium spp.] Impagidinium cf. sphaericum [Impagidinium spp.] Impagidinium strialatum [Impagidinium spp.] Impagidinium spp. [Impagidinium spp.] Lingulodinium hemicystum Lingulodinium sp. A [Lingulodinium spp.] Lingulodinium spp. [Lingulodinium spp.] Nematosphaeropsis labyrinthus Operculodinium centrocarpum sensu Wall and Dale 1966 Operculodinium cf. israelianum [Operculodinium spp.] Operculodinium longispinigerum Operculodinium israelianum [Operculodinium spp.] Operculodinium spp. [Operculodinium spp.] Cy st of Pentapharsodinium dalei Polysphaeridium zoharyi Spiniferites bentorii Spiniferites bulloideus [Spinif erites spp.] Spiniferites delicatus [Spiniferites spp.] Spiniferites hyperacanthus Spiniferites cf. ludhamensis [Spiniferites spp.] Spiniferites membranaceus [Spiniferites mirabilis] Spiniferites mirabilis Spiniferites pacificus Spiniferites pachydermus [Spiniferites spp.] Spiniferites ramosus Spiniferites spp. [Spiniferites spp.] Tuberculodinium vancampoae

Autotrophic Achomosphaera spp. Bitectatodinium spongium Dapsilidinium pastielsii Impagidinium aculeatum Impagidinium paradoxum Impagidinium patulum Impagidinium spp. Lingulodinium spp. Nematosphaeropsis labyrinthus Operculodinium centrocarpum Operculodinium longispinigerum Polysphaeridium zoharyi Spiniferites bentorii Spiniferites hyperacanthus Spiniferites miraiblis Spiniferites ramosus Spiniferites spp. Tuberculodinium vancampoae

ro

-p

re

lP

Heterotrophic Brigantedinium spp. Dubridinium spp. Echinidinium spp. Lejeunecysta sabrina Cy st of Protoperidinium spp. Quinquecuspis concreta Selenopemphix nephroides Selenopemphix quanta Selenopemphix undulata Stelladinium reidii Trinovantedinium applanatum

Jo

Calcareous cysts and others Cladopyxis spp. Cyclopsiella spp. Cymatiosphaera Halodinium major Pediastrum Scrippsiella trochoidea

ur

na

Heterotrophic Brigantedinium spp. [Brigantedinium spp.] Cy st of Diplopelta parva [Brigantedinium spp.] Lejeunecysta sabrina Cy st of Polykrikos kofoidii Pre-ency sted Protoperidinium [Cyst of Protoperidinium spp.] Quinquecuspis concreta Selenopemphix nephroides Selenopemphix quanta Stelladinium stellatum [Stelladinium reidii] Trinovantedinium applanatum Votadinium calvum [Cyst of P. oblongum] Votadinium spinosum [Cyst of Protoperidinium spp.]

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Cyst taxa from Kaw amura (2002, 2004)

Heterotrophic Brigantedinium cariacoense [Brigantedinium spp.] Brigantedinium irregulare [Brigantedinium spp.] Brigantedinium simplex [Brigantedinium spp.] Brigantedinium sp. A [Brigantedinium spp.] Brigantedinium spp. [Brigantedinium spp.] Cryodinium cf. meridianum Dubridinium caperatum [Dubridinium spp.] Dubridinium cavatum [Dubridinium spp.] Echinidinium aculeatum [Echinidinium spp.] Echinidinium granulatum [Echinidinium spp.] Echinidinium transparatum [Echinidinium spp.] Echinidinium spp. [Echinidinium spp.] Cy st of Pentaplacodinium saltonense Cy st of Protoperidinium spp. [Cyst of Protoperidinium spp.] Lejeunecysta sabrina Leipokatium invisitatum Quinquecuspis concreta Selenopemphix nephroides Selenopemphix quanta Selenopemphix tholus Selenopemphix undulata Stelladinium reidii Trinovantedinium applanatum Votadinium elongatum [Votadinium spp.] Votadinium pontifossatum [Votadinium spp.] Votadinium spp. [Votadinium spp.]

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Conflict of interest statement

We declare that we have no financial and non-financial interests and personal relationships with other people or organizations that can inappropriately influence our work and this

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Journal Pre-proof Author statement

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All authors collected the data, contributed to interpretation of results and discussion, and edited this manuscript.

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Journal Pre-proof Highlights 

The first detailed study of dinoflagellate cysts and controlling environmental parameters in surface sediments across the South China Sea was performed.

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The highest cyst concentrations occur in the upwelling area off southern Vietnam, whereas the lowest was off Luzon.

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SST, chl-a concentrations, and water depth were identified as primary controlling factors

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in cyst spatial distributions.

Brigantedinium spp. dominate regions having high sea-surface temperature.

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Higher abundances of Impagidinium spp. were found in the areas influenced by the

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Kuroshio Current.

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